Abstract
This study investigated the therapeutic potential of probiotic bifidobacteria, isolated from Iranian fermented dairy products, in a hyperlipidemic animal model. Bifidobacterium strains were extracted from traditional dairy samples and screened using physiological and phenotypic examinations, 16S rRNA analysis, and probiotic properties such as tolerance to gastrointestinal juice, antimicrobial activity, and antibiotic susceptibility. The ability of the screened bifidobacteria to reduce serum and liver lipids in vivo was tested using male Wistar rats. Six strains of bifidobacteria were isolated from traditional Iranian fermented dairy. These strains showed promising in vitro activity in lowering triglyceride and cholesterol, tolerance to simulated gastrointestinal juice, the ability to adhere to Caco-2 cells, acceptable antibiotic susceptibility, and a broad spectrum of antibacterial activity. The diet supplemented with isolated bifidobacteria significantly reduced serum total cholesterol (TC), triglyceride (TG), low-density lipoprotein cholesterol (LDL-C), liver tissue lipid levels, and hepatic enzymes in animals when compared to a high-fat diet without strains (p < 0.01). Additionally, the potential probiotic-supplemented diet significantly increased bile acid excretion in the feces and upregulated hepatic CYP7A1 expression levels (p < 0.05), while NPC1L1, ACAT2, and MTP gene expressions in small intestinal cells were downregulated (p < 0.05). Bifidobacteria isolated from Iranian traditional dairy showed potential for use in the production of fermented foods that have hypolipemic activity in the host.
Similar content being viewed by others
Data availability
The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information files. Should any raw data files be needed in another format they are available from the corresponding author upon reasonable request.
References
Aktas B, De Wolfe TJ, Safdar N, Darien BJ, Steele JL (2016) The impact of Lactobacillus casei on the composition of the cecal microbiota and innate immune system is strain specific. PLoS ONE 11:e0156374
Asl ZR, Sepehri G, Salami M (2019) Probiotic treatment improves the impaired spatial cognitive performance and restores synaptic plasticity in an animal model of Alzheimer’s disease. Behav Brain Res 376:112183
Baumgartner S, Bruckert E, Gallo A, Plat J (2020) The position of functional foods and supplements with a serum LDL-C lowering effect in the spectrum ranging from universal to care-related CVD risk management. Atherosclerosis 311:116–123
Bilige M, Liu W, Rina W, Wang L, Sun T, Wang J, Li H, Zhang H (2009) Evaluation of potential probiotics properties of the screened Lactobacillus isolated from home-made koumiss in Mongolia. Ann Microbiol 59:493–498
Cao K, Zhang K, Ma M, Ma J, Tian J, Jin Y (2021) Lactobacillus mediates the expression of NPC1L1, CYP7A1, and ABCG5 genes to regulate cholesterol. Food Sci Nutr 9:6882–6891
Casarotti SN, Carneiro BM, Todorov SD, Nero LA, Rahal P, Penna ALB (2017) In vitro assessment of safety and probiotic potential characteristics of Lactobacillus strains isolated from water buffalo mozzarella cheese. Ann Microbiol 67:289–301
Companys J, Pla-Pagà L, Calderón-Pérez L, Llauradó E, Solà R, Pedret A, Valls RM (2020) Fermented dairy products, probiotic supplementation, and cardiometabolic diseases: a systematic review and meta-analysis. Adv Nutr 11:834–863
de la Visitación N, Robles-Vera I, Toral M, Duarte J (2019) Protective effects of probiotic consumption in cardiovascular disease in systemic lupus erythematosus. Nutrients 11:2676
de Moura e Dias M, dos Reis Louzano SA, da Conceição LL, da Conceição Fernandes R, de Oliveira Mendes TA, Pereira SS, de Oliveira LL, Gouveia Peluzio MDC (2021) Antibiotic followed by a potential probiotic increases brown adipose tissue, reduces biometric measurements, and changes intestinal microbiota phyla in obesity. Probiotics Antimicrob Proteins 10:1–11
DiRienzo DB (2014) Effect of probiotics on biomarkers of cardiovascular disease: implications for heart-healthy diets. Nutr Rev 72:18–29
Famouri F, Shariat Z, Hashemipour M, Keikha M, Kelishadi R (2017) Effects of probiotics on nonalcoholic fatty liver disease in obese children and adolescents. J Pediatr Gastroenterol Nutr 64:413–417
Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Gao Y, Li D (2018) Screening of lactic acid bacteria with cholesterol-lowering and triglyceride-lowering activity in vitro and evaluation of probiotic function. Ann Microbiol 68:537–545
Gong WH, Zheng WX, Wang J, Chen SH, Pang B, Hu XM, Cao XL (2012) Coexistence of hyperlipidemia and acute cerebral ischemia/reperfusion induces severe liver damage in a rat model. World J Gastroenterol 18:4934–4939
Greene JD, Klaenhammer TR (1994) Factors involved in adherence of lactobacillus to human Caco-2 cells. Appl Environ Microbiol 60:4487–4494
Huang Y, Wang X, Wang J, Wu F, Sui Y, Yang L, Wang Z (2013) Lactobacillus plantarum strains as potential probiotic cultures with cholesterol-lowering activity. J Dairy Sci 96:2746–2753
Huang Y, Zheng Y (2010) The probiotic Lactobacillus acidophilus reduces cholesterol absorption through the down-regulation of Niemann-Pick C1-like 1 in Caco-2 cells. Br J Nutr 103:473–478
Ishimwe N, Daliri EB, Lee BH, Fang F, Du G (2015) The perspective on cholesterol-lowering mechanisms of probiotics. Mol Nutr Food Res 59:94–105
Jia B, Zou Y, Han X, Bae JW, Jeon CO (2022) Gut microbiome-mediated mechanisms for reducing cholesterol levels: implications for ameliorating cardiovascular disease. Trends Microbiol 30:1–14
Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, Okano M, Kagoshima M, Tsuchida T (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64:636–643
Khan A, Ding Z, Ishaq M, Bacha AS, Khan I, Hanif A, Li W, Guo X (2021) Understanding the effects of gut microbiota dysbiosis on nonalcoholic fatty liver disease and the possible probiotics role: recent updates. Int J Biol Sci 17:818–829
Locket PL, Gallaher DD (1989) An improved procedure for bile acid extraction and purification and tissue distribution in the rat. Lipids 24:221–223
Mandal V, Sen SK, Mandal NC (2009) Effect of prebiotics on bacteriocin production and cholesterol lowering activity of Pediococcus acidilactici LAB 5. World J Microbiol Biotechnol 25:1837–1847
Nami Y, Bakhshayesh RV, Manafi M, Hejazi MA (2019) Hypocholesterolaemic activity of a novel autochthonous potential probiotic Lactobacillus plantarum YS5 isolated from yogurt. LWT 111:876–882
Nguyen T, Kang J, Lee M (2007) Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int J Food Microbiol 113:358–361
Nido SA, Shituleni SA, Mengistu BM, Liu Y, Khan AZ, Gan F, Kumbhar S, Huang K (2016) Effects of selenium-enriched probiotics on lipid metabolism, antioxidative status, histopathological lesions, and related gene expression in mice fed a high-fat diet. Biol Trace Elem Res 171:399–440
Nourizadeh R, Sepehri B, Abbasi A, Sayyed R, Khalili L (2022) Impact of probiotics in modulation of gut microbiome. In Microbiome-Gut-Brain Axis: Implications on Health, 401–490
Olas B (2020) Probiotics, prebiotics and synbiotics—a promising strategy in prevention and treatment of cardiovascular diseases? Int J Mol Sci 21:9737
Ondee T, Pongpirul K, Visitchanakun P, Saisorn W, Kanacharoen S, Wongsaroj L, Kullapanich C, Ngamwongsatit N, Settachaimongkon S, Somboonna N (2021) Lactobacillus acidophilus LA5 improves saturated fat-induced obesity mouse model through the enhanced intestinal Akkermansia muciniphila. Sci Rep 11:6367
Oniszczuk A, Oniszczuk T, Gancarz M, Szymańska J (2021) Role of gut microbiota, probiotics and prebiotics in the cardiovascular diseases. Molecules 26:1172–1175
Rudel LL, Morris M (1973) Determination of cholesterol using o-phthalaldehyde. J Lipid Res 14:364–366
Saboori B, Shahidi F, Hedayati S, Javadmanesh A (2022) Investigating the probiotic properties and antimicrobial activity of lactic acid bacteria isolated from an Iranian fermented dairy product. Kashk Foods 11:3904
Shin HS, Park SY, Lee DK, Kim SA, An HM, Kim JR, Kim MJ, Cha MG, Lee SW, Kim KJ (2010) Hypocholesterolemic effect of sonication-killed Bifidobacterium longum isolated from healthy adult Koreans in high cholesterol fed rats. Arch Pharmacal Res 33:1425–1431
Sivamaruthi BS, Fern LA, Hj DSNRP, Chaiyasut C (2020) The influence of probiotics on bile acids in diseases and aging. Biomed Pharmacother 128:110310
Song X, Liu Y, Zhang X, Weng P, Zhang R, Wu Z (2023) Role of intestinal probiotics in the modulation of lipid metabolism: implications for therapeutic treatments. Food Sci Nutr 12:1439–1449
Xie N, Cui Y, Yin Y-N, Zhao X, Yang J-W, Wang Z-G, Fu N, Tang Y, Wang X-H, Liu X-W (2011) Effects of two Lactobacillus strains on lipid metabolism and intestinal microflora in rats fed a high-cholesterol diet. BMC Complement Altern Med 11:1–25
Xue L, He J, Gao N, Lu X, Li M, Wu X, Liu Z, Jin Y, Liu J, Xu J (2017) Probiotics may delay the progression of nonalcoholic fatty liver disease by restoring the gut microbiota structure and improving intestinal endotoxemia. Sci Rep 7:1–15
Yasmin I, Saeed M, Khan WA, Khaliq A, Chughtai MFJ, Iqbal R, Tehseen S, Naz S, Liaqat A, Mehmood T (2020) In vitro probiotic potential and safety evaluation (hemolytic, cytotoxic activity) of Bifidobacterium strains isolated from raw camel milk. Microorganisms 8:354–358
Zanotti I, Turroni F, Piemontese A, Mancabelli L, Milani C, Viappiani A, Prevedini G, Sanchez B, Margolles A, Elviri L (2015) Evidence for cholesterol-lowering activity by Bifidobacterium bifidum PRL2010 through gut microbiota modulation. Appl Microbiol Biotechnol 99:7721–7731
Zeng XQ, Pan DD, Zhou PD (2011) Functional characteristics of Lactobacillus fermentum F1. Curr Microbiol 62:27–31
Zhang W, Yang J, Zhou Z, Deng L, Lai S, Liu H, Zhong Z, Fu H, Ren Z, Shen L (2022) Screening and evaluation of lactic acid bacteria with probiotic potential from local Holstein raw milk. Front Microbiol 13:918774
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
All applicable international guidelines for the care and use of animals were followed. Animal studies in this experiment were carried out strictly according to the rules of the Animal Welfare and Research Ethics Committee of Islamic Azad University (Arak, Iran), and the permit number was IR.IAU.ARAK.REC.1399.018.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Afshar, N., Amini, K., Mohajerani, H. et al. Evaluation of probiotic bifidobacteria strains from Iranian traditional dairy products for their anti-hyperlipidemic potential. Folia Microbiol (2024). https://doi.org/10.1007/s12223-023-01124-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12223-023-01124-1